Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination

Iana H. Haralambieva, Richard B Kennedy, Whitney L. Simon, Krista M. Goergen, Diane E. Grill, Inna G. Ovsyannikova, Gregory A. Poland

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.

Original languageEnglish (US)
Article numbere0191812
JournalPLoS One
Volume13
Issue number1
DOIs
StatePublished - Jan 1 2018

Fingerprint

Measles
Humoral Immunity
MicroRNAs
microRNA
humoral immunity
Individuality
B-lymphocytes
Vaccination
B-Lymphocytes
vaccination
Cells
biomarkers
T-lymphocytes
vaccines
Measles virus
T-cells
Biomarkers
antibodies
Viruses
phosphatidylinositols

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination. / Haralambieva, Iana H.; Kennedy, Richard B; Simon, Whitney L.; Goergen, Krista M.; Grill, Diane E.; Ovsyannikova, Inna G.; Poland, Gregory A.

In: PLoS One, Vol. 13, No. 1, e0191812, 01.01.2018.

Research output: Contribution to journalArticle

Haralambieva, Iana H. ; Kennedy, Richard B ; Simon, Whitney L. ; Goergen, Krista M. ; Grill, Diane E. ; Ovsyannikova, Inna G. ; Poland, Gregory A. / Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination. In: PLoS One. 2018 ; Vol. 13, No. 1.
@article{aa024e68fb4148e9a37acb92d3398d78,
title = "Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination",
abstract = "Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.",
author = "Haralambieva, {Iana H.} and Kennedy, {Richard B} and Simon, {Whitney L.} and Goergen, {Krista M.} and Grill, {Diane E.} and Ovsyannikova, {Inna G.} and Poland, {Gregory A.}",
year = "2018",
month = "1",
day = "1",
doi = "10.1371/journal.pone.0191812",
language = "English (US)",
volume = "13",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "1",

}

TY - JOUR

T1 - Differential miRNA expression in B cells is associated with inter-individual differences in humoral immune response to measles vaccination

AU - Haralambieva, Iana H.

AU - Kennedy, Richard B

AU - Simon, Whitney L.

AU - Goergen, Krista M.

AU - Grill, Diane E.

AU - Ovsyannikova, Inna G.

AU - Poland, Gregory A.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.

AB - Background MicroRNAs are important mediators of post-transcriptional regulation of gene expression through RNA degradation and translational repression, and are emerging biomarkers of immune system activation/response after vaccination. Methods We performed Next Generation Sequencing (mRNA-Seq) of intracellular miRNAs in measles virus-stimulated B and CD4+ T cells from high and low antibody responders to measles vaccine. Negative binomial generalized estimating equation (GEE) models were used for miRNA assessment and the DIANA tool was used for gene/target prediction and pathway enrichment analysis. Results We identified a set of B cell-specific miRNAs (e.g., miR-151a-5p, miR-223, miR-29, miR-15a-5p, miR-199a-3p, miR-103a, and miR-15a/16 cluster) and biological processes/pathways, including regulation of adherens junction proteins, Fc-receptor signaling pathway, phosphatidylinositol-mediated signaling pathway, growth factor signaling pathway/pathways, transcriptional regulation, apoptosis and virus-related processes, significantly associated with neutralizing antibody titers after measles vaccination. No CD4+ T cell-specific miRNA expression differences between high and low antibody responders were found. Conclusion Our study demonstrates that miRNA expression directly or indirectly influences humoral immunity to measles vaccination and suggests that B cell-specific miRNAs may serve as useful predictive biomarkers of vaccine humoral immune response.

UR - http://www.scopus.com/inward/record.url?scp=85041198660&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85041198660&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0191812

DO - 10.1371/journal.pone.0191812

M3 - Article

C2 - 29381765

AN - SCOPUS:85041198660

VL - 13

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 1

M1 - e0191812

ER -